Relaxed natural selection alone does not permit transposable element expansion within 4,000 generations in Escherichia coli

Genetica

Volumn 139, Issue 7, 2011, Pages 895-902

  Plague, Gordon R ^a,b   Dougherty, Kevin M ^a,c   Boodram, Krystal S ^a   Boustani, Samantha E ^a   Cao, Huansheng ^a   Manning, Sarah R ^a   McNally, Camille C ^a  

^a FORDHAM UNIVERSITY   (United States)

^b STATE UNIVERSITY OF NEW YORK AT POTSDAM   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Experimental evolution; Genetic drift; IS element; Pathogenic bacteria

Indexed keywords

ARTICLE; BACTERIAL GENOME; BIOLOGICAL MODEL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC DRIFT; GENETIC SELECTION; GENETICS; MOLECULAR EVOLUTION; TRANSPOSON;

DNA TRANSPOSABLE ELEMENTS; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENETIC DRIFT; GENOME, BACTERIAL; MODELS, GENETIC; MUTAGENESIS, INSERTIONAL; SELECTION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 79960838650     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10709-011-9593-x     Document Type: Article

References (62)

1. Bergthorsson U, Ochman H (1995) Heterogeneity of genome sizes among natural isolates of Escherichia coli. J Bacteriol 177: 5784-5789.
2. Bergthorsson U, Ochman H (1998) Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol Biol Evol 15: 6-16.
3. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462.
4. Brinster S, Lamberet G, Staels B, Trieu-Cuot P, Gruss A, Poyart C (2009) Type II fatty acid synthesis is not a suitable antibiotic target for Gram-positive pathogens. Nature 458: 83-86.
5. Capy P, Gasperi G, Biémont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity 85: 101-106.
6. Chain PSG, Hu P, Malfatti SA, Radnedge L, Larimer F, Vergez LM, Worsham P, Chu MC, Andersen GL (2006) Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. J Bacteriol 188: 4453-4463.
7. Chandler M, Mahillon J (2002) Insertion sequences revisited. In: Craig NL, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II, vol 5/6. ASM Press, Washington, pp 305-366.
8. Chao L, McBroom SM (1985) Evolution of transposable elements: an IS10 insertion increases fitness in Escherichia coli. Mol Biol Evol 2: 359-369.
9. Conlon KM, Humphreys H, O'Gara JP (2004) Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J Bacteriol 186: 6208-6219.
10. Cooper VS, Schneider D, Blot M, Lenski RE (2001) Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol 183: 2834-2841.
11. Cornelis G (1980) Transposition of Tn951 (Tnlac) and cointegrate formation are thermosensitive processes. J Gen Microbiol 117: 243-247.
12. Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601-603.
13. Dougherty KM, Plague GR (2008) Transposable element loads in a bacterial symbiont of weevils are extremely variable. Appl Environ Microbiol 74: 7832-7834.
14. Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Taourit S, Bocs S, Boursaux-Eude C, Chandler M, Dassa E, Derose R, Derzelle S, Freyssinet G, Gaudriault S, Givaudan A, Médigue C, Lanois A, Powell K, Siguier P, Wingate V, Zouine M, Glaser P, Boemare N, Danchin A, Kunst F (2003) The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat Biotechnol 21: 1307-1313.
15. Dykhuizen DE (1990) Experimental studies of natural selection in bacteria. Annu Rev Ecol Syst 21: 373-398.
16. Edwards RJ, Brookfield JFY (2003) Transiently beneficial insertions could maintain mobile DNA sequences in variable environments. Mol Biol Evol 20: 30-37.
17. Elena SF, Ekunwe L, Hajela N, Oden SA, Lenski RE (1998) Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica 102(103): 349-358.
18. Fraser C, Hanage WP, Spratt BG (2007) Recombination and the nature of bacterial speciation. Science 315: 476-480.
19. Haren L, Bétermier M, Polard P, Chandler M (1997) IS911-mediated intramolecular transposition is naturally temperature sensitive. Mol Microbiol 25: 531-540.
20. Herzer PJ, Inouye S, Inouye M, Whittam TS (1990) Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol 172: 6175-6181.
21. Kang Y, Durfee T, Glasner JD, Qiu Y, Frisch D, Winterberg KM, Blattner FR (2004) Systematic mutagenesis of the Escherichia coli genome. J Bacteriol 186: 4921-4930.
22. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge.
23. Kimura M, Ohta T (1969) The average number of generations until fixation of a mutant gene in a finite population. Genetics 61: 763-771.
24. Kothary MH, Babu US (2001) Infective dose of foodborne pathogens in volunteers: a review. J Food Saf 21: 49-73.
25. Kretschmer PJ, Cohen SN (1979) Effect of temperature on translocation frequency of the Tn3 element. J Bacteriol 139: 515-519.
26. Leavis HL, Willems RJL, van Wamel WJB, Schuren FH, Caspers MPM, Bonten MJM (2007) Insertion sequence-driven diversification creates a globally dispersed emerging multiresistant subspecies of E. faecium. PLoS Pathog 3: e7.
27. Lederberg J (2004) E. coli K-12. Microbiol Today 31: 116.
28. Lee B-M, Park Y-J, Park D-S, Kang H-W, Kim J-G, Song E-S, Park I-C, Yoon U-H, Hahn J-H, Koo B-S, Lee G-B, Kim H, Park H-S, Yoon K-O, Kim J-H, Jung C-h, Koh N-H, Seo J-S, Go S-J (2005) The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res 33: 577-586.
29. Lenski RE, Rose MR, Simpson SC, Tadler SC (1991) Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2, 000 generations. Am Nat 138: 1315-1341.
30. Lind PA, Berg OG, Andersson DI (2010) Mutational robustness of ribosomal protein genes. Science 330: 825-827.
31. Lynch M (2007) The origins of genome architecture. Sinauer Associates, Sunderland.
32. Lynch M, Conery JS (2003) The origins of genome complexity. Science 302: 1401-1404.
33. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor.
34. Moran NA, Plague GR (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14: 627-633.
35. Moran NA, Wernegreen JJ (2000) Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol 15: 321-326.
36. Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119: 736-747.
37. Newton ILG, Bordenstein SR (2011) Correlations between bacterial ecology and mobile DNA. Curr Microbiol 62: 198-208.
38. Nuzhdin SV (1999) Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107: 129-137.
39. Ochman H, Davalos LM (2006) The nature and dynamics of bacterial genomes. Science 311: 1730-1733.
40. Ochman H, Moran NA (2001) Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292: 1096-1098.
41. Ochman H, Wilson AC (1987) Evolutionary history of enteric bacteria. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. ASM Press, Washington, pp 1649-1654.
42. Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246: 96-98.
43. Ohtsubo Y, Genka H, Komatsu H, Nagata Y, Tsuda M (2005) High-temperature-induced transposition of insertion elements in Burkholderia multivorans ATCC 17616. Appl Environ Microbiol 71: 1822-1828.
44. Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284: 604-607.
45. Papadopoulos D, Schneider D, Meier-Eiss J, Arber W, Lenski RE, Blot M (1999) Genomic evolution during a 10, 000-generation experiment with bacteria. Proc Natl Acad Sci USA 96: 3807-3812.
46. Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, Holden MT, Churcher CM, Bentley SD, Mungall KL, Cerdeño-Tarraga AM, Temple L, James K, Harris B, Quail MA, Achtman M, Atkin R, Baker S, Basham D, Bason N, Cherevach I, Chillingworth T, Collins M, Cronin A, Davis P, Doggett J, Feltwell T, Goble A, Hamlin N, Hauser H, Holroyd S, Jagels K, Leather S, Moule S, Norberczak H, O'Neil S, Ormond D, Price C, Rabbinowitsch E, Rutter S, Sanders M, Saunders D, Seeger K, Sharp S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Unwin L, Whitehead S, Barrell BG, Maskell DJ (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35: 32-40.
47. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: 2002-2007.
48. Pfaffl MW (2004) Quantification strategies in real-time PCR. In: Bustin SA (ed) A-Z of quantitative PCR, vol 2-3. International University Line Press, La Jolla, pp 87-120.
49. Pfeifer F, Blaseio U (1990) Transposition burst of the ISH27 insertion element family in Halobacterium halobium. Nucleic Acids Res 18: 6921-6925.
50. Plague GR, Dunbar HE, Tran PL, Moran NA (2008) Extensive proliferation of transposable elements in heritable bacterial symbionts. J Bacteriol 190: 777-779.
51. Riley M (1993) Functions of the gene products of Escherichia coli. Microbiol Rev 57: 862-952.
52. Russell DG (2005) Where to stay inside the cell: a homesteader's guide to intracellular parasitism. In: Cossart P, Boquet P, Normark S, Rappuoli R (eds) Cellular microbiology, 2nd edn. ASM Press, Washington, pp 227-253.
53. Safi H, Barnes PF, Lakey DL, Shams H, Samten B, Vankayalapati R, Howard ST (2004) IS6110 functions as a mobile, monocyte-activated promoter in Mycobacteriumtuberculosis. Mol Microbiol 52: 999-1012.
54. Schmitz-Esser S, Tischler P, Arnold R, Montanaro J, Wagner M, Rattei T, Horn M (2010) The genome of the amoeba symbiont "Candidatus Amoebophilus asiaticus" reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J Bacteriol 192: 1045-1057.
55. Song Y, Tong Z, Wang J, Wang L, Guo Z, Han Y, Zhang J, Pei D, Zhou D, Qin H, Pang X, Han Y, Zhai J, Li M, Cui B, Qi Z, Jin L, Dai R, Chen F, Li S, Ye C, Du Z, Lin W, Wang J, Yu J, Yang H, Wang J, Huang P, Yang R (2004) Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res 11: 179-197.
56. Todd ECD, Greig JD, Bartleson CA, Michaels BS (2008) Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 4. Infective doses and pathogen carriage. J Food Prot 71: 2339-2373.
57. Touchon M, Rocha EPC (2007) Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol 24: 969-981.
58. Treves DS, Manning S, Adams J (1998) Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 15: 789-797.
59. Wahl LM, Gerrish PJ (2001) The probability that beneficial mutations are lost in populations with periodic bottlenecks. Evolution 55: 2606-2610.
60. Whittam TS, Ake SE (1993) Genetic polymorphisms and recombination in natural populations of Escherichia coli. In: Takahata N, Clark AG (eds) Mechanisms of molecular evolution. Sinauer Associates, Sunderland, pp 223-245.
61. Woyke T, Teeling H, Ivanova NN, Huntemann Ml, Richter M, Gloeckner FO, Boffelli D, Anderson IJ, Barry KW, Shapiro HJ, Szeto E, Kyrpides NC, Mussmann M, Amann R, Bergin C, Ruehland C, Rubin EM, Dubilier N (2006) Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443: 950-955.
62. Yang F, Yang J, Zhang X, Chen L, Jiang Y, Yan Y, Tang X, Wang J, Xiong Z, Dong J, Xue Y, Zhu Y, Xu X, Sun L, Chen S, Nie H, Peng J, Xu J, Wang Y, Yuan Z, Wen Y, Yao Z, Shen Y, Qiang B, Hou Y, Yu J, Jin Q (2005) Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery. Nucleic Acids Res 33: 6445-6458.